Journal of Pest Science

, Volume 86, Issue 2, pp 245–251 | Cite as

Host discrimination ability in the tephritid parasitoid Psyttalia concolor (Hymenoptera: Braconidae)

  • Giovanni Benelli
  • Gabriele Gennari
  • Angelo Canale
Original Paper

Abstract

Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) is a koinobiont larval-pupal endoparasitoid of many Tephritidae of economic importance. Little has been reported on the ability of females to discriminate between healthy and parasitized hosts, as well as parasitized versus superparasitized larvae. Two-choice bioassays were conducted to evaluate the preferences of P. concolor naïve females for healthy or single-parasitized/superparasitized C. capitata larvae, as well as the host discrimination ability among medfly larvae which had been superparasitized by the same wasp or by a conspecific one. Psyttalia concolor preferred to oviposit in a unparasitized C. capitata larva than in a self-parasitized one. Females also showed an innate ability to discriminate between larvae parasitized twice or only once, preferring the latter. This ability helps the female to optimise its oviposition decisions by deliberately avoiding superparasitized hosts, since it is known that they give a lower return in offspring number and quality than do singly parasitized hosts. Our findings contribute to a better knowledge of the P. concolor host location behaviour and also to improve its mass-rearing technique through a rational management of the host/parasitoid ratio and the host exposure time. Indeed, the proper setting of these parameters allows to reduce the fraction of single-parasitized and heavily superparasitized larvae and to enhance P. concolor rearing in terms of parasitoid offspring.

Keywords

Biological control Mediterranean fruit fly Olive fruit fly Opiinae Superparasitism 

References

  1. Bakker K, Peulet PH, Visser ME (1989) The ability to distinguish between hosts containing different numbers of parasitoid eggs by the solitary parasitoid Leptopilina heterotoma (Thomson) (Hym., Cynip.). Neth J Zool 40:514–520CrossRefGoogle Scholar
  2. Benelli G, Canale A (2012) Learning of visual cues in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). Biocontrol 57:767–777CrossRefGoogle Scholar
  3. Benelli G, Bonsignori G, Stefanini C, Canale A (2012a) Courtship and mating behaviour in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae): the role of wing fanning. J Pest Sci 85:55–63CrossRefGoogle Scholar
  4. Benelli G, Flamini G, Canale A, Cioni PL, Conti B (2012b) Toxicity evaluation of different essential oil formulations against the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera Tephritidae). Crop Prot 42:223–229CrossRefGoogle Scholar
  5. Canale A (1998) Effect of parasitoid/host ratio on superparasitism of Ceratitis capitata (Wiedemann) larvae (Diptera: Tephritidae) by Opius concolor Szépligeti (Hymenoptera: Braconidae). Frustula Entomol 21:137–148Google Scholar
  6. Canale A, Benelli G (2012) Impact of mass-rearing on the host-seeking behaviour and parasitism by the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). J Pest Sci 85:65–74CrossRefGoogle Scholar
  7. Canale A, Raspi A (2000) Host location and oviposition behaviour in Opius concolor Szépligeti (Hymenoptera, Braconidae). Entomol Probl 31:25–32Google Scholar
  8. Carpita A, Canale A, Raffaelli A, Saba A, Benelli G, Raspi A (2012) (Z)-9-Tricosene identified in rectal glands extracts of Bactrocera oleae males: first evidence of a male-produced female attractant in olive fruit fly. Naturwissenschaften 99:77–81PubMedCrossRefGoogle Scholar
  9. Chow A, Mackauer M (1996) Sequential allocation of offspring sexes in the hyperparasitoid wasp, Dendrocerus carpenteri. Anim Behav 51:859–870CrossRefGoogle Scholar
  10. Cloutier C, Lothar AD, Bauduin F (1984) Host discrimination in the aphid parasitoid Aphidius nigripes. Can J Zool 62:1367–1372CrossRefGoogle Scholar
  11. Daane KM, Johnson MW (2010) Olive fruit fly: managing an ancient pest in modern times. Annu Rev Entomol 55:151–169PubMedCrossRefGoogle Scholar
  12. Darrouzet E, Bignon, Chevrier C (2007) Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp. Entomol Exp Appl 123:279–285CrossRefGoogle Scholar
  13. Dorn S, Beckage NE (2007) Superparasitism in gregarious Hymenopteran parasitoids: ecological, behavioural and physiological perspectives. Physiol Entomol 32:199–211CrossRefGoogle Scholar
  14. Fisher RC (1971) Aspects of the physiology of endoparasitic Hymenoptera. Biol Rev 46:243–278CrossRefGoogle Scholar
  15. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, PrincetonGoogle Scholar
  16. González PI, Montoya P, Perez-Lachaud G, Cancino J, Liedo P (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biol Control 40:320–326CrossRefGoogle Scholar
  17. Goubault M, Crespi L, Boivin G, Poinsot D, Nénon JP, Cortesero AM (2004) Intraspecific variations in host discrimination behavior in the pupal parasitoid Pachycrepoideus vindemmiae Rondani (Hymenoptera: Pteromalidae). Environ Entomol 33:362–369CrossRefGoogle Scholar
  18. Goubault M, Cortesero AM, Paty C, Fourrier J, Dourlot S, Le Ralec A (2011) Abdominal sensory equipment involved in external host discrimination in a solitary parasitoid wasp. Microsc Res Tech 74:1145–1153PubMedCrossRefGoogle Scholar
  19. Greany PD, Hawke SD, Carlysle TC, Anthony DW (1977) Sense organs in the ovipositor of Biosteres (Opius) longicaudatus, a parasite of the caribbean fruit fly Anastrepha suspensa. Ann Entomol Soc Am 70:319–321Google Scholar
  20. Gu H, Wang Q, Dorn S (2003) Superparasitism in Cotesia glomerata: response of hosts and consequences for parasitoids. Ecol Entomol 28:422–431CrossRefGoogle Scholar
  21. Harvey JA, Harvey IF, Thompson DJ (1993) The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens (Hymenoptera: Ichneumonidae). Ecol Entomol 18:203–208CrossRefGoogle Scholar
  22. Hegazi E, Khafagi W (2008) The effects of host age and superparasitism by the parasitoid, Microplitis rufiventris on the cellular and humoral immune response of Spodoptera littoralis larvae. J Invert Pathol 98:79–84CrossRefGoogle Scholar
  23. Jacas JA, Budia F, Rodriguez-Cerezo E, Vinuela E (1997) Virus-like particles in the poison gland of the parasitic wasp Opius concolor. Ann Appl Biol 130:587–592CrossRefGoogle Scholar
  24. Kitano H, Nakatsuji N (1978) Resistance of Apanteles eggs to haemocytic encapsulation by their habitual host, Pieris. J Insect Physiol 24:261–271CrossRefGoogle Scholar
  25. Mackauer M, Chau A (2001) Adaptive self superparasitism in a solitary parasitoid wasp: the influence of clutch size on offspring size. Funct Ecol 15:335–343CrossRefGoogle Scholar
  26. Mahmoud AMA, Lim UT (2008) Host discrimination and interspecific competition of Trissolcus nigripedius and Telenomus gifuensis (Hymenoptera: Scelionidae), sympatric parasitoids of Dolycoris baccarum (Heteroptera: Pentatomidae). Biol Control 45:337–343CrossRefGoogle Scholar
  27. Mayhew PJ, van Alphen JJM (1999) Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Anim Behav 58:131–141PubMedCrossRefGoogle Scholar
  28. Meyhöfer R, Casas J (1999) Vibratory stimuli in host location by parasitic wasps. J Insect Physiol 45:967–971PubMedCrossRefGoogle Scholar
  29. Moore D, Ridout MS (1987) Avoidance of super-parasitism of stem-boring larvae by Chasmodon apterus [Hym.: Braconidae]. Entomophaga 32:299–302CrossRefGoogle Scholar
  30. Outreman Y, Le Ralec A, Plantegenest M, Chaubet B, Pierre JS (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. J Insect Physiol 47:339–348PubMedCrossRefGoogle Scholar
  31. Plantegenest M, Outreman J, Goubault M, Wajnberg E (2004) Parasitoids flip a coin before deciding to superparasitize. J Anim Ecol 73:802–806CrossRefGoogle Scholar
  32. Rabinovich JE, Jorda MT, Bernstein C (2000) Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera: Scelionidae), a parasitoid of triatomine eggs. Behav Ecol Sociobiol 48:308–315CrossRefGoogle Scholar
  33. Raspi A, Canale A (2000) Effect of superparasitism on Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) second instar larvae by Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). Redia LXXXIII:123–131Google Scholar
  34. Santolamazza-Carbone S, Rodriguez-Illamola A, Cordero Rivera A et al (2004) Host finding and host discrimination ability in Anaphes nitens Girault, an egg parasitoid of the Eucalyptus snout-beetle Gonipterus scutellatus Gyllenhal. Biol Control 29:24–33CrossRefGoogle Scholar
  35. Sprinthall RC (2003) Basic statistical analysis. Pearson Education, BostonGoogle Scholar
  36. Tepedino VJ (1988) Host discrimination in Monodontomerus obsoletus Fabricius (Hymenoptera: Torymidae), a parasite of the Alfalfa leafcutting bee Megachile rotundata (Fabricius) (Hymenoptera:Megachilidae). J N Y Entomol Soc 96:113–118Google Scholar
  37. Thompson SN (1986) Effect of the insect parasite Hyposoter axiguae (Viereck) on the carbohydrate metabolism of its host, Trichoplusia ni (Hubner). J Insect Physiol 32:287–293CrossRefGoogle Scholar
  38. Ueno T, Tanaka T (1994) Can a female parasitoid recognize a previously rejected host? Anim Behav 47:988–990CrossRefGoogle Scholar
  39. van Alphen JJM, Jervis MA (1996) Foraging behaviour. In: Jervis M, Kidd N (eds) Insect natural enemies. Chapman & Hall, LondonGoogle Scholar
  40. van Alphen JJM, Nell HW (1981) Superparasitism and host discrimination by Asobara tabida Nees (Braconidae, Alysiinae), a larval parasitoid of Drosophila. Neth J Zool 32:232–260CrossRefGoogle Scholar
  41. van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 35:59–79PubMedCrossRefGoogle Scholar
  42. van Baaren J, Boivin G, Nénon JP (1994) Intra- and interspecific host discrimination in two closely related egg parasitoids. Oecologia 100:325–330CrossRefGoogle Scholar
  43. van Dijken MJ, Waage JK (1987) Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomol Exp Appl 43:183–192CrossRefGoogle Scholar
  44. Varaldi J, Fouilllet P, Boulétreau M, Fleury F (2005) Superparasitism acceptance and patch-leaving mechanisms in parasitoids: a comparison between two sympatric wasps. Anim Behav 69:1227–1234CrossRefGoogle Scholar
  45. Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–86CrossRefGoogle Scholar
  46. Vinson SB, Guillot FS (1972) Host marking: source of a substance that results in host discrimination in insect parasitoids. Entomophaga 17:241–245CrossRefGoogle Scholar
  47. Vinson SB, Sroka P (1978) Effects of superparasitism by a solitary endoparasitoid on the host, parasitoid and field samplings. Southwest Entomol 3:299–301Google Scholar
  48. Wang XY, Yang ZQ, Gould JR, Wu H, Ma JH (2010) Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer. Biol Control 52:24–29CrossRefGoogle Scholar
  49. Wang XG, Johnson MW, Yokoyama VY, Pickett CH, Daane KM (2011) Comparative evaluation of two olive fruit fly parasitoids under varying abiotic conditions. Biocontrol 56:283–293CrossRefGoogle Scholar
  50. Weisser WW, Houston AI (1993) Host discrimination in parasitic wasps: When is it advantageous? Funct Ecol 7:27–39CrossRefGoogle Scholar
  51. Wharton RA (1997) Generic relationships of opiine Braconidae (Hymenoptera) parasitic on fruit-infesting Tephritidae (Diptera). Contrib Am Entomol Inst 30:1–53Google Scholar
  52. Yamada YY, Miyamoto K (1998) Payoff from self and conspecific superparasitism in a dryinid parasitoid, Haplogonatopus atratus. Oikos 81:209–216CrossRefGoogle Scholar
  53. Yamada YY, Sugaura K (2003) Evidence for adaptive self-superparasitism in the drynid parasitoid Haplogonatopus atratus when conspecifics are present. Oikos 103:175–181CrossRefGoogle Scholar
  54. Zhang L, Raspi A (1999) Learning behaviour of Opius concolor Szépligeti (Hymenoptera: Braconidae) in host discrimination. Entomol Sin 6:259–266Google Scholar
  55. Zhang JH, Gu LQ, Wang CZ (2010) Superparasitism behavior and host discrimination of Campoletis chloridae (Ichneumonidae: Hymenoptera) toward Mythimna separata (Noctuidae: Lepidoptera). Environ Entomol 39:1249–1254PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Giovanni Benelli
    • 1
  • Gabriele Gennari
    • 1
  • Angelo Canale
    • 1
  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly

Personalised recommendations